Niche Construction and Evolution

Richard Lewontin

The niche-construction perspective was introduced to evolutionary biology in the 1980s through a series of seminal essays by Harvard evolutionary biologist Richard Lewontin (1-3), and has gathered momentum over recent years.

Niche construction is the process whereby organisms, through their metabolism, their activities, and their choices, modify their own and/or others’ niches (4). For instance, numerous animals manufacture nests, burrows, holes, webs, and pupal cases; plants change levels of atmospheric gases and modify nutrient cycles; fungi and bacteria decompose organic matter; and bacteria fix nutrients. However, the defining characteristic of niche construction is not organism-driven modification of the environment per se (a special case known as ‘perturbational niche construction’), but rather modification of the organism’s niche (5). Hence the term ‘niche construction’ includes such cases as dispersal, migration and habitat selection, where organisms relocate in space to modify the environments that they experience (known as ‘relocational niche construction’).

Inceptive niche construction applies to cases in which organisms initiate change in an environmental factor, either through perturbation of their surroundings or opportunistic dispersal into a new location. However, if an environmental factor is already changing, or has changed, organisms may oppose or cancel out that change, a process labelled counteractive niche construction. For instance, many wasps and bees will engage in temperature regulation of their nests, heating it up through muscular activity in the cold, and placing droplets of water on the surface, allowing it to cool through evaporation, in the heat. Counteractive niche construction is therefore conservative or stabilizing, and it functions to protect organisms from shifts in factors away from states to which they have been adapted.

Advocates of the niche-construction perspective seek to explain the adaptive complementarity of organism and environment in terms of a dynamic, reciprocal interaction between the processes of natural selection and niche construction. Evolution is based on networks of causation and feedback in which organisms drive environmental change and organism-modified environments subsequently select organisms.

Niche-construction theory contrasts with conventional conceptualizations of evolution. In standard models, leaving aside complications such as coevolution and habitat selection, adaptation is a process by which natural selection shapes organisms to fit preexisting environmental ‘templates’.

The causal arrow points in one direction only: environments, the source of selection, determine the features of living creatures. According to George Williams: ‘Adaptation is always asymmetrical; organisms adapt to their environment, never vice versa’ (6).

Beaver dam

The distinction between this evolutionary perspective and that emphasizing niche construction is illustrated by the familiar example of the beaver. Standard evolutionary theory models the evolutionary consequences of beaver dam building in the same way as other aspects of beaver phenotypes: solely in terms of fitness ‘payoffs’ to the underlying genes; that is, selection favors dam-building alleles over their alternatives.

Dawkins explains that dam building is an extended phenotypic trait (7) but a central theme of his argument is that extended phenotypic adaptations evolve in a manner that is no different from any other adaptations.

Advocates of NCT regard this stance as unsatisfactory, both because it misses part of the causal story and because it discourages consideration of certain forms of selective feedback within evolution. When a beaver builds a dam and lodge, creating a lake and influencing river flow, it not only affects the propagation of dam-building genes but it dramatically changes its local environment, affecting nutrient cycling, decomposition dynamics, the structure of the riparian zone, and plant and community composition and diversity (8). It follows that beaver dam building must also transform selection acting on a host of other beaver traits, influencing subsequent beaver evolution. The active agency of beavers in constructing these modified selection pressures and thereby acting as co-directors of their own evolution (not to mention that of other species) currently goes unrecognized.

Often the modifications produced by niche-constructing organisms persist for longer than the individual constructors, continuing to modulate the impact of environment on subsequent generations of the population, a legacy described as an ‘ecological inheritance‘ (5). For instance, modified selection pressures will remain in the beaver’s environment just so long as the dam, lake, and lodge remain. Given that dams are frequently maintained by families of beavers for decades, (8) that could be considerably longer than the lifetime of an individual beaver. Likewise a single mound system can last many termite lives, and the changes that earthworms produce in the soil can last many generations. While standard evolutionary theory recognizes that environments can exhibit constantcy across generations, this is not treated as an inheritance. From the niche-construction perspective, offspring inherit two legacies from their ancestors, genes and a modified selective environment.

To some extent it is possible to study this feedback using established evolutionary theory, for instance through models of habitat selection, co-evolution, maternal inheritance or indirect genetic effects. Nonetheless, the magnitude and significance of niche construction remains underappreciated, in part because standard evolutionary theory does not encourage attention to such phenomena (1,9).

Advocates of niche construction theory believe that it is useful to think of niche construction as an evolutionary process in its own right. Niche construction is regarded as an initiator of evolutionary change rather than merely the end product of earlier selection. One practical advantage of treating niche construction as both a unitary phenomenon and evolutionary cause is that it brings with it a fresh perspective, novel hypotheses, and new methods that can stimulate research within evolutionary biology (4). The niche-construction perspective is of value precisely because foregrounds the impact of organisms on selective environments. Although this position remains controversial (10-12), the niche construction perspective is rapidly growing, precisely because researchers from multiple disciplines find it useful.

Many researchers have explored the evolutionary ramifications of niche construction by developing and analyzing mathematical models (4,13-19). All such analyses conclude that niche construction is evolutionarily consequential. The analyses suggest that the effects of niche construction can override external sources of selection to create new evolutionary trajectories, which lead to the fixation of otherwise deleterious alleles, the support of stable equilibria where none are expected, and the elimination of what would otherwise be stable polymorphisms. Even niche construction that only weakly affects resource dynamics can significantly alter both ecological and evolutionary patterns. This is because traits whose fitness depends on alterable sources of selection co-evolve with traits that alter sources of selection. Such co-evolution results in evolutionary dynamics that are very different from what would occur if each trait had evolved in isolation. For instance, populations evolving in response to features of the environment modified by their ancestors can exhibit any one of several effects: continuing to evolve in the same direction after selection has stopped or reversed—a lag effect; inertia effects (no noticeable evolutionary response to selection for a number of generations)—another kind of lag effect; and opposite and sudden catastrophic responses to selection.

Other theoretical studies corroborate and extend these findings. For instance, niche construction allows the persistence of organisms in inhospitable environmental conditions that would otherwise lead to their extinction (20). Niche-construction traits can drive themselves to fixation by simultaneously generating selection that favours ‘recipient’ trait alleles and linkage disequilibrium between niche-construction and recipient trait alleles (18). Niche construction has been shown to profoundly influence the dynamics, competition, and diversity of metapopulations (21). Moreover, costly niche-constructing traits can be favored because of the benefits of the niche construction that will accrue to distant descendants (22). Thus, evolutionary fitness ultimately depends not on the number of offspring, or even of grand-offspring, but on the long-term genetic legacy of alleles or genotypes within a population. The value of the niche constrution perspective is that it stimulates these kind of analyses, and leads to such insights.

Arabidopsis thaliana

Donohue (23) showed experimentally how niche construction frequently occurs in plants through developmental plasticity, allowing them to determine the selective environments that they or their offspring experience. For instance, seed dispersal ability frequently determines the competitive environment experienced by seeds, seedlings and adult plants. Flowering time determines the seasonal environment that the seeds experience.

Germination timing effectively involves habitat choice in plants, since certain environmental conditions must be present to break dormancy, and additional environmental conditions must be present to enable germination after dormancy is broken. For these reasons, it is reasonable to regard traits such as seed dispersal ability, flowering time and germination timing as niche-constructing traits. Donohue describes an experimental study with Arabidopsis thaliana showing how two niche-constructing traits—flowering and germination time—influence selection, phenotypic expression and genetic variation, resulting in novel life-history expression (23).

Forest fire

Similarly, flammability has been portrayed as a niche-constructing trait,affecting the evolution of fireresistance and resprouting rate in pine and chapparal trees, which promote forest fires through accumulating oils and litter (24,25).

More generally, in addition to modifying the selective environments of populations, niche construction modifies the developmental environments of individuals, resulting in systematic changes to the phenotypic expression of inherited genes. Sometimes niche construction may modify the shape of the relevant norm of reaction, for instance, by reducing the range of developmental environments to which juveniles are exposed (11). Nests, burrows, mounds and similar structures all tend to buffer environmental variation, making temperature, humidity, exposure to wind and sunlight more uniform.

Termite nest internal structure

If a developmental environment does become more uniform as a result of niche construction, then alleles that have equivalent phenotypic effects in, say, burrow-rearing environments but not in a broader class of environments, become selectively equivalent. The heritability of the trait associated with any such allele is typically affected by the reduction in environmental variation. Conversely, niche construction can result in exposure to a broader range of developmental conditions: (11) for example, when parents relocate, their offspring are likely to be exposed to novel developmental environments. Similar arguments have been made with respect to phenotypic plasticity (9).

Woodpecker Finch

Niche construction also provides a (non-Lamarckian) route by which acquired characteristics can influence the selective environment. Acquired characteristics are of particular significance to vertebrate evolution. The Galapagos woodpecker finch provides an example (4). These birds create a woodpecker-like niche by learning to use a cactus spine or similar implement to peck for insects under bark (26). While true woodpeckers’ (Picidae) bills are adaptive traits fashioned by natural selection for grubbing, the woodpecker finch’s capacity to use spines to grub for insects is not an adaptation. Rather, this finch exploits a more general and flexible adaptation, namely the capacity to learn the skills necessary to grub in its environment by using cactus spines, or similar implements.

The finch’s use of spines develops reliably as a consequence of its ability to interact with itsenvironment in a manner that allows it to benefit from its own experience, but this is not guaranteed by the presence of naturally selected genes, nor does it depend on social learning (26). However, the finch’s learning opens up resources in the bird’s environment that would be unavailable to it otherwise, and it is therefore an example of niche construction. This niche-constructing behaviour probably created a stable selection pressure that subsequently favoured a bill able to manipulate tools rather than the sharp, pointed bill and long tongue characteristic of most woodpeckers. While the information acquired by individuals through ontogenetic processes cannot be inherited because it is lost when they die, processes such as learning can nonetheless still be of considerable importance to subsequent generations because learned knowledge can guide niche construction.

Coral reef

More generally, any mechanism of phenotypic plasticity in conjunction with reliably present signals from the environment may generate the same niche-constructing activity generation by generation, with evolutionary consequences, without the activity itself being an adaptation, and without the necessity of any tight correspondence between genetic and phenotypic variation (9,27,28) For instance, corals influence water speeds, the erosive impact of waves, siltation rates, and so forth,(29) an instance of niche construction, but their capacity to do so is in itself affected by water flow.

Bower bird and nest

The effect of acquired characters has been considerably enhanced by social learning, which allows animals to learn from each other. Hundreds of species of mammals, birds and fishes are now known to learn socially (30,31), allowing novel learned traits to sweep through populations, exposing individuals to novel selection pressures. There is already considerable interest among evolutionary biologists in the role that imprinting, song learning, habitat imprinting, cultural transmission and various other forms of learning, play in speciation, the evolution of adaptive specializations, adaptive radiations, the colonization of new habitats, brood parasitism and sexual selection in vertebrates. (9,32-38) From the niche-construction perspective, learning in general, and social learning in particular, is likely to exert a widespread influence on animal evolution. This point is of particular relevance to the human sciences.